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Title: Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon

Abstract

Oral iron administration in African children can increase the risk for infections. However, it remains unclear to what extent supplementary iron affects the intestinal microbiome. We here explored the impact of iron preparations on microbial growth and metabolism in the well-controlled TNO's in vitro model of the large intestine (TIM-2). The model was inoculated with a human microbiota, without supplementary iron, or with 50 or 250 μmol/L ferrous sulfate, 50 or 250 μmol/L ferric citrate, or 50 μmol/L hemin. High resolution responses of the microbiota were examined by 16S rDNA pyrosequencing, microarray analysis, and metagenomic sequencing. The metabolome was assessed by fatty acid quantification, gas chromatography-mass spectrometry (GC-MS), and 1H-NMR spectroscopy. Cultured intestinal epithelial Caco-2 cells were used to assess fecal water toxicity. Microbiome analysis showed, among others, that supplementary iron induced decreased levels of Bifidobacteriaceae and Lactobacillaceae, while it caused higher levels of Roseburia and Prevotella. Metagenomic analyses showed an enrichment of microbial motility-chemotaxis systems, while the metabolome markedly changed from a saccharolytic to a proteolytic profile in response to iron. Branched chain fatty acids and ammonia levels increased significantly, in particular with ferrous sulfate. Importantly, the metabolite-containing effluent from iron-rich conditions showed increased cytotoxicity to Caco-2 cells. Inmore » conclusion, our explorations indicate that in the absence of host influences, iron induces a more hostile environment characterized by a reduction of microbes that are generally beneficial, and increased levels of bacterial metabolites that can impair the barrier function of a cultured intestinal epithelial monolayer.« less

Authors:
 [1];  [2];  [3];  [1];  [4];  [5];  [6];  [7];  [7];  [7];  [1];  [1];  [3];  [1]
  1. Radboud Univ., Nijmegen (Netherlands)
  2. Radboud Univ., Nijmegen (Netherlands); Univ. of Utrecht (Netherlands); Federal Univ. of Rio de Janeiro (Brazil)
  3. TNO Innovation for Life, Zeist (Netherlands)
  4. NIZO food research, Kernhemseweg Ede (Netherlands)
  5. Argonne National Lab. (ANL), Argonne, IL (United States); Univ. of Chicago, Lemont, IL (United States)
  6. Illumina Inc., Little Chesterford (United Kingdom); DNA digest, Future Business Centre, Cambridge (United Kingdom)
  7. Illumina Inc., Little Chesterford (United Kingdom)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1258646
Resource Type:
Accepted Manuscript
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Volume: 6; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; in vitro fermentation; iron supplementation; gutmicrobiome; metabolome; metagenome; toxicity; SCFA; BCFA

Citation Formats

Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, and Tjalsma, Harold. Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon. United States: N. p., 2016. Web. doi:10.3389/fmicb.2015.01481.
Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, & Tjalsma, Harold. Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon. United States. https://doi.org/10.3389/fmicb.2015.01481
Kortman, Guus A. M., Dutilh, Bas E., Maathuis, Annet J. H., Engelke, Udo F., Boekhorst, Jos, Keegan, Kevin P., Nielsen, Fiona G. G., Betley, Jason, Weir, Jacqueline C., Kingsbury, Zoya, Kluijtmans, Leo A. J., Swinkels, Dorine W., Venema, Koen, and Tjalsma, Harold. Wed . "Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon". United States. https://doi.org/10.3389/fmicb.2015.01481. https://www.osti.gov/servlets/purl/1258646.
@article{osti_1258646,
title = {Microbial Metabolism Shifts Towards an Adverse Profile with Supplementary Iron in the TIM-2 In vitro Model of the Human Colon},
author = {Kortman, Guus A. M. and Dutilh, Bas E. and Maathuis, Annet J. H. and Engelke, Udo F. and Boekhorst, Jos and Keegan, Kevin P. and Nielsen, Fiona G. G. and Betley, Jason and Weir, Jacqueline C. and Kingsbury, Zoya and Kluijtmans, Leo A. J. and Swinkels, Dorine W. and Venema, Koen and Tjalsma, Harold},
abstractNote = {Oral iron administration in African children can increase the risk for infections. However, it remains unclear to what extent supplementary iron affects the intestinal microbiome. We here explored the impact of iron preparations on microbial growth and metabolism in the well-controlled TNO's in vitro model of the large intestine (TIM-2). The model was inoculated with a human microbiota, without supplementary iron, or with 50 or 250 μmol/L ferrous sulfate, 50 or 250 μmol/L ferric citrate, or 50 μmol/L hemin. High resolution responses of the microbiota were examined by 16S rDNA pyrosequencing, microarray analysis, and metagenomic sequencing. The metabolome was assessed by fatty acid quantification, gas chromatography-mass spectrometry (GC-MS), and 1H-NMR spectroscopy. Cultured intestinal epithelial Caco-2 cells were used to assess fecal water toxicity. Microbiome analysis showed, among others, that supplementary iron induced decreased levels of Bifidobacteriaceae and Lactobacillaceae, while it caused higher levels of Roseburia and Prevotella. Metagenomic analyses showed an enrichment of microbial motility-chemotaxis systems, while the metabolome markedly changed from a saccharolytic to a proteolytic profile in response to iron. Branched chain fatty acids and ammonia levels increased significantly, in particular with ferrous sulfate. Importantly, the metabolite-containing effluent from iron-rich conditions showed increased cytotoxicity to Caco-2 cells. In conclusion, our explorations indicate that in the absence of host influences, iron induces a more hostile environment characterized by a reduction of microbes that are generally beneficial, and increased levels of bacterial metabolites that can impair the barrier function of a cultured intestinal epithelial monolayer.},
doi = {10.3389/fmicb.2015.01481},
journal = {Frontiers in Microbiology},
number = ,
volume = 6,
place = {United States},
year = {Wed Jan 06 00:00:00 EST 2016},
month = {Wed Jan 06 00:00:00 EST 2016}
}

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Works referenced in this record:

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journal, August 2013


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journal, December 2014

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  • Journal of Microbiological Methods, Vol. 107
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Advances and perspectives in in vitro human gut fermentation modeling
journal, January 2012


Nutritional iron deficiency in patients with chronic illnesses
journal, December 2007


Different Human Gut Models Reveal the Distinct Fermentation Patterns of Arabinoxylan versus Inulin
journal, October 2013

  • Van den Abbeele, Pieter; Venema, Koen; Van de Wiele, Tom
  • Journal of Agricultural and Food Chemistry, Vol. 61, Issue 41
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Gut Microbial Activity, Implications for Health and Disease: The Potential Role of Metabolite Analysis
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A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010

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  • DOI: 10.1038/nature08821

Nutritional immunity: transition metals at the pathogen–host interface
journal, July 2012

  • Hood, M. Indriati; Skaar, Eric P.
  • Nature Reviews Microbiology, Vol. 10, Issue 8
  • DOI: 10.1038/nrmicro2836

The Effect of the Undigested Fraction of Maize Products on the Activity and Composition of the Microbiota Determined in a Dynamic in Vitro Model of the Human Proximal Large Intestine
journal, December 2009


The Effect of Various Inulins and Clostridium difficile on the Metabolic Activity of the Human Colonic Microbiota in vitro
journal, November 2003

  • van Nuenen, Marleen H. M. C.; Diederick Meyer, P.; Venema, Koen
  • Microbial Ecology in Health and Disease, Vol. 15, Issue 2-3
  • DOI: 10.1080/08910600310018959

Fermentation in the human large intestine and the available substrates
journal, May 1987

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  • The American Journal of Clinical Nutrition, Vol. 45, Issue 5
  • DOI: 10.1093/ajcn/45.5.1243

Evaluating the microbial diversity of an in vitro model of the human large intestine by phylogenetic microarray analysis
journal, November 2010

  • Rajilić-Stojanović, Mirjana; Maathuis, Annet; Heilig, Hans G. H. J.
  • Microbiology, Vol. 156, Issue 11
  • DOI: 10.1099/mic.0.042044-0

Major players on the microbial stage: why archaea are important
journal, February 2011


Nutritional iron turned inside out: intestinal stress from a gut microbial perspective
journal, November 2014

  • Kortman, Guus A. M.; Raffatellu, Manuela; Swinkels, Dorine W.
  • FEMS Microbiology Reviews, Vol. 38, Issue 6
  • DOI: 10.1111/1574-6976.12086

Linking phylogenetic identities of bacteria to starch fermentation in an in vitro model of the large intestine by RNA-based stable isotope probing
journal, April 2009


The domain Archaea in human mucosal surfaces
journal, September 2012


Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites
journal, August 2012


Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine
journal, May 2009


Interactions Between the Microbiota and the Immune System
journal, June 2012


Use of a three-stage continuous culture system to study the effect of mucin on dissimilatory sulfate reduction and methanogenesis by mixed populations of human gut bacteria.
journal, January 1988


Alpha-keto acids are novel siderophores in the genera Proteus, Providencia, and Morganella and are produced by amino acid deaminases.
journal, January 1993


Diet and faecal flora in the newborn: casein and whey proteins.
journal, December 1989

  • Balmer, S. E.; Scott, P. H.; Wharton, B. A.
  • Archives of Disease in Childhood, Vol. 64, Issue 12
  • DOI: 10.1136/adc.64.12.1678

Diet and faecal flora in the newborn: lactoferrin.
journal, December 1989

  • Balmer, S. E.; Scott, P. H.; Wharton, B. A.
  • Archives of Disease in Childhood, Vol. 64, Issue 12
  • DOI: 10.1136/adc.64.12.1685

Diet and faecal flora in the newborn: iron.
journal, December 1991

  • Balmer, S. E.; Wharton, B. A.
  • Archives of Disease in Childhood, Vol. 66, Issue 12
  • DOI: 10.1136/adc.66.12.1390

Depletion of luminal iron alters the gut microbiota and prevents Crohn's disease-like ileitis
journal, November 2010


Gut Microbiota in Health and Disease
journal, July 2010

  • Sekirov, Inna; Russell, Shannon L.; Antunes, L. Caetano M.
  • Physiological Reviews, Vol. 90, Issue 3
  • DOI: 10.1152/physrev.00045.2009

Faecal Microbiota and Short-Chain Fatty Acid Levels in Faeces from Infants with Cow‘s Milk Protein Allergy
journal, January 2011

  • Thompson-Chagoyan, Oscar C.; Fallani, Matteo; Maldonado, José
  • International Archives of Allergy and Immunology, Vol. 156, Issue 3
  • DOI: 10.1159/000323893

Effects of probiotics and antibiotics on the intestinal homeostasis in a computer controlled model of the large intestine
journal, January 2012

  • Rehman, Ateequr; Heinsen, Femke-Anouska; Koenen, Marjorie E.
  • BMC Microbiology, Vol. 12, Issue 1
  • DOI: 10.1186/1471-2180-12-47

Iron Availability Increases the Pathogenic Potential of Salmonella Typhimurium and Other Enteric Pathogens at the Intestinal Epithelial Interface
journal, January 2012


The Global Hidden Hunger Indices and Maps: An Advocacy Tool for Action
journal, June 2013


Functions of Bacterial Flagella
journal, January 1996


The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Côte d'Ivoire
journal, October 2010

  • Zimmermann, Michael B.; Chassard, Christophe; Rohner, Fabian
  • The American Journal of Clinical Nutrition, Vol. 92, Issue 6
  • DOI: 10.3945/ajcn.110.004564

Galacto-Oligosaccharides Have Prebiotic Activity in a Dynamic In Vitro Colon Model Using a 13C-Labeling Technique
journal, May 2012

  • Maathuis, Annet J. H.; van den Heuvel, Ellen G.; Schoterman, Margriet H. C.
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